Skip to main content
SpringerLink
Log in

Effects of partial destruction of the suprachiasmatic nuclei on two circadian parameters: wheel-running activity and short-day induced testicular regression

  • Published:
Journal of Comparative Physiology A Aims and scope Submit manuscript

Summary

Many circadian rhythms in mammals are regulated by the suprachiasmatic nuclei located in the anterior hypothalamus. The suprachiasmatic nuclei are a heterogeneous population of neurons loosely segregated into regions. In an effort to determine if a regional specificity of control of different circadian rhythms exists within the SCN, the effect of small electrolytic lesions of the suprachiasmatic nuclei was examined on two parameters which are known to depend on the circadian system for their normal expression: wheel-running activity and short-day induced testicular regression. While some SCN lesions altered both the circadian rhythm of locomotor activity and the normal temporal pattern of gonadal regression on short-days, other partial lesions of the suprachiasmatic nuclei were found to effect one parameter without effecting the other. Detailed histological analysis of the neural damage sustained by the suprachiasmatic nuclei did not indicate an obvious regional specificity of function within the nuclei. However, the results do suggest that functionally specific neural pathways emerging from the suprachiasmatic nuclei carry circadian information to independent neural circuits responsible for locomotor activity and neuroendocrine-gonadal function.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

Abbreviations

SCN :

suprachiasmatic nucleus

SCG :

superior cervical ganglion

NAT :

N-acetyltransferase

LD :

light/dark cycle

DD :

constant darkness

τ :

circadian period

ψ :

phase angle of entrainment

HRP :

horseradish peroxidase

SEM :

standard error of the mean

vPVN :

hypothalamic paraventricular nucleus

DMH :

hypothalamic dorsomedial nucleus

PVT :

thalamic paraventricular nucleus

IMLN :

intermediolateral nucleus

References

  • Aghajanian GK, Bloom FE, Sheard MH (1969) Electron mibacroscopy of degeneration within the serotonin pathway of the rat brain. Brain Res 13:266–273

    Google Scholar 

  • Berk ML, Finkelstein JA (1981) An autoradiographic determination of the efferent projections of the suprachiasmatic nucleus of the hypothalamus. Brain Res 226:1–13

    Google Scholar 

  • Berndtson WE, Desjardins C (1974) Circulating LH and FSH levels and testicular function in hamsters during light deprivation and subsequent stimulation. Endocrinology 95:195–205

    Google Scholar 

  • Bowers CW, Zigmond RE (1980) Electrical stimulation of the cervical sympathetic trunks mimics the effects of darkness on the activity of serotonin: N-acetyltransferase in the rat pineal. Brain Res 185:435–440

    Google Scholar 

  • Bowers CW, Zigmond RE (1982) The influence of the frequency and pattern of sympathetic nerve activity on serotonin N-acetyltransferase in the rat pineal gland. J Physiol 30:279–296

    Google Scholar 

  • Carmichael MS, Nelson R, Zucker I (1981) Hamster activity and estrous cycles: Control by a single versus multiple circadian oscillator(s). Proc Natl Acad Sci USA 78:7830–7834

    Google Scholar 

  • Elliott JA (1976) Circadian rhythms and photoperiodic time measurement in mammals. Fed Proc 35:2339–2346

    Google Scholar 

  • Elliott JA, Goldman BD (1981) Seasonal reproduction: Photoperiodism and biological clocks. In: Adler NT (ed) Neuroendocrinology of reproduction, physiology and behavior. Plenum Press, New York, pp 377–423

    Google Scholar 

  • Ellis GB, McKlveen RE, Turek FW (1982) Dark pulses affect the circadian rhythm of activity in hamsters kept in constant light. Am J Physiol 242:R44-R50

    Google Scholar 

  • Enright JT (1980) The timing of sleep and wakefulness. Springer Berlin Heidelberg, New York

    Google Scholar 

  • Eskes GA, Wilkinson M, Rusak B (1982) Neural control of hamster seasonal breeding cycles. Biol Reprod 26 (Suppl 1):97A

    Google Scholar 

  • Follett BK, Robinson JE, Simpson SM, Harlow CR (1981) Photoperiodic time measurement and gonadotropin secretion in quail. In: Follett BK, Follett DE (eds) Biological clocks in seasonal reproductive cycles. Wright, Bristol, pp 185–201

    Google Scholar 

  • Gaston S, Menaker M (1967) Photoperiodic control of hamster testes. Science 158:925–928

    Google Scholar 

  • Gilbey MP, Coote JH, Fleetwood-Walker S, Peterson DF (1982) The influence of the paraventricular-spinal pathway, and oxytocin and vasopressin on sympathetic preganglionic neurons. Brain Res 251:283–290

    Google Scholar 

  • Glass JD, Lynch GR (1982) Evidence for a brain site of melatonin action in the white-footed mouse,Peromyscus leucopus. Neuroendocrinology 34:1–6

    Google Scholar 

  • Green DJ, Gillette R (1982) Circadian rhythm of firing rate recorded from single cells in the rat suprachiasmatic brain slice. Brain Res 245:198–200

    Google Scholar 

  • Groos G, Hendriks J (1982) Circadian rhythms in electrical discharge of rat suprachiasmatic neurones recorded in vitro. Neurosci Lett 34:283–288

    Google Scholar 

  • Guldner F-H (1976) Synaptology of the rat suprachiasmatic nucleus. Cell Tissue Res 165:509–544

    Google Scholar 

  • Hendrickson AE, Wagoner N, Cowan WM (1972) An autoradiographic and electron microscopic study of retino-hypothalamic connections. Z Zellforsch 135:1–26

    Google Scholar 

  • Hoffman RA, Reiter RJ (1965) Pineal gland: Influence on gonads of male hamsters. Science 148:1609–1611

    Google Scholar 

  • Hoffmann K (1981) Photoperiodism in vertebrates. In: Aschoff J (ed) Handbook of behavioral neurobiology, vol 4. Biological rhythms, Plenum Press, New York, pp 449–473

    Google Scholar 

  • Hosoya Y (1980) The distribution of spinal projection neurons in the hypothalamus of the rat, studied with the HRP method. Exp Brain Res 40:79–87

    Google Scholar 

  • Inouye ST, Kawamura H (1979) Persistence of circadian rhythmicity in a mammalian hypothalamic ‘island’ containing the suprachiasmatic nucleus. Proc Natl Acad Sci USA 76:5962–5966

    Google Scholar 

  • Klein DC, Smoot R, Weller JL, Higa S, Markey SP, Creed GJ, Jacobawitz DM (1983) Lesions of the parventricular nucleus area of the hypothalamus disrupt the suprachiasmatic-spinal cord circuit in the melatonin rhythm generating system. Brain Res Bull 10:647–652

    Google Scholar 

  • Kucera P, Favrod P (1979) Suprachiasmatic nucleus projection to mesencephalic central grey in the woodmouse (Apodemussylvaticus L.) Neurosci 4:1705–1715

    Google Scholar 

  • Kuypers HGJM, Maisky VA (1975) Retrograde axonal transport of horseradish peroxidase from spinal cord to brain stem cell groups in the cat. Neurosci Lett 1:9–14

    Google Scholar 

  • Luiten PM, Room P (1980) Interrelations between lateral, dorsomedial and ventromedial hypothalamic nuclei in the rat; An HRP study. Brain Res 190:321–332

    Google Scholar 

  • Lydic R, Albers HE, Tepper B, Moore-Ede MC (1982) Threedimensional structure of the mammalian suprachiasmatic nuclei: A comparative study of five species. J Comp Neurol 204:225–237

    Google Scholar 

  • McC Brooks C, Ishikawa T, Koizumi K (1975) Autonomic system control of the pineal gland and the role of this complex in the integration of body function. Brain Res 87:181–190

    Google Scholar 

  • Moore RY (1973) Retinohypothalamic projection in mammals: a comparative study. Brain Res 49:403–409

    Google Scholar 

  • Moore RY (1983) Organization and function of a central nervous system circadian oscillator: the suprachiasmatic nuclei. Fed Proc 42:2783–2789

    Google Scholar 

  • Moore RY, Eichler VB (1972) Loss of a circadian adrenal corticosterone rhythm following suprachiasmatic lesions in the rat. Brain Res 42:201–206

    Google Scholar 

  • Moore RY, Klein DC (1974) Visual pathways and the central neural control of a circadian rhythm in pineal serotonin N-acetyltransferase activity. Brain Res 71:17–33

    Google Scholar 

  • Moore RY, Lenn NJ (1972) A retinohypothalamic projection in the rat. J Comp Neurol 146:1–14

    Google Scholar 

  • Mosko SA, Moore RY (1979a) Retinohypothalamic tract development: Alteration by suprachiasmatic lesions in the neonatal rat. Brain Res 164:1–15

    Google Scholar 

  • Mosko SA, Moore RY (1979b) Neonatal suprachiasmatic nucleus lesions: Effects on the development of circadian rhythms in the rat. Brain Res 164:17–38

    Google Scholar 

  • Nishino H, Koizumi K, McC Brooks C (1976) The role of the suprachiasmatic nuclei of the hypothalamus in the production of circadian rhythms. Brain Res 112:45–59

    Google Scholar 

  • Nishio T, Shiosaka S, Nakagawa H, Sakumoto T, Satoh K (1979) Circadian feeding rhythms after hypothalamic knifecut isolating suprachiasmatic nucleus. Physiol Behav 23:763–769

    Google Scholar 

  • Nunez AA, Casati MJ (1979) The role of efferent connections of the suprachiasmatic nucleus in the control of circadian rhythms. Behav Neurol Biol 25:263–267

    Google Scholar 

  • Nunez AA, Stephan FK (1977) The effects of hypothalamic knife-cuts on drinking rhythms and the estrous cycle of the rat. Behav Biol 20:224–234

    Google Scholar 

  • Pickard GE (1982) The afferent connections of the suprachiasmatic nucleus of the golden hamster with emphasis on the retinohypothalamic projection. J Comp Neurol 211:65–83

    Google Scholar 

  • Pickard GE, Silverman AJ (1979) The effects of photoperiod on hypothalamic luteinizing hormone-releasing hormone (LHRH) in the male hamster. J Endocrinology 83:421–428

    Google Scholar 

  • Pickard GE, Silverman AJ (1981) Direct retinal projections to the hypothalamus, piriform cortex and accessory optic nuclei in the golden hamster as demonstrated by a sensitive anterograde horseradish peroxidase technique. J Comp Neurol 196:155–172

    Google Scholar 

  • Pickard GE, Turek FW (1982) Splitting of the circadian rhythm of activity is abolished by unilateral lesions of the suprachiasmatic nuclei. Science 215:1119–1121

    Google Scholar 

  • Pickard GE, Turek FW (1983a) The suprachiasmatic nuclei: Two circadian clocks? Brain Res 268:201–210

    Google Scholar 

  • Pickard GE, Turek FW (1983b) The hypothalamic paraventricular nucleus mediates the photoperiodic control of reproduction but not the effects of light on the circadian rhythm of activity. Neurosci Lett 43:67–72

    Google Scholar 

  • Rando TA, Bowers CW, Zigmond RE (1981) Localization of neurons in the rat spinal cord which project to the superior cervical ganglion. J Comp Neurol 196:73–83

    Google Scholar 

  • Reiter RJ (1980) The pineal and its hormones in the control of reproduction in mammals. Endocrine Rev 1:109–113

    Google Scholar 

  • Reiter RJ, Vaughan MK, Blask D, Johnson LY (1975) Pineal methoxyindoles: New evidence concerning their function in the control of pineal-mediated changes in the reproductive physiology of male golden hamsters. Endocrinology 96:206–213

    Google Scholar 

  • Rietveld WJ, Kooij M, Flory W, Aardoom OR (1982) The effect of dorsomedial hypothalamic nucleus lesions on the circadian control of food intake, locomotor activity, body temperature and estrous cycle in rats. IRCS Biochem 10:905–906

    Google Scholar 

  • Rusak B, Groos G (1982) Suprachiasmatic stimulation phase shifts rodent circadian rhythms. Science 215:1407–1409

    Google Scholar 

  • Rusak B, Morin LP (1976) Testicular responses to photoperiod are blocked by lesions of the suprachiasmatic nuclei in golden hamsters. Biol Reprod 15:366–374

    Google Scholar 

  • Rusak B, Zucker I (1979) Neural regulation of circadian rhythms. Physiol Rev 59:449–526

    Google Scholar 

  • Saper CB, Loewy AD, Swanson LW, Cowan WM (1976) Direct hypothalamo-autonomic connections. Brain Res 117:305–312

    Google Scholar 

  • Schwartz WJ, Gainer H (1977) Suprachiasmatic nucleus: Use of 14 C-labeled deoxyglucose uptake as a functional marker. Science 197:1089–1091

    Google Scholar 

  • Schwartz WJ, Davidson LC, Smith CB (1980) In vivo metabolic activity of a putative circadian oscillator, the rat suprachiasmatic nucleus. J Comp Neurol 189:157–167

    Google Scholar 

  • Shibata S, Oomura Y, Kita H, Hattori K (1982) Circadian rhythmic changes of neuronal activity in the suprachiasmatic nucleus of the rat hypothalamic slice. Brain Res 247:154–158

    Google Scholar 

  • Sofronniew MV, Weindl A (1982) Neuroanatomical organization and connections of the suprachiasmatic nucleus. In: Aschoff A, Daan S, Groos G (eds) Vertebrate circadian systems. Springer, Berlin Heidelberg New York, pp 75–86

    Google Scholar 

  • Stephan FK Berkley KJ, Moss RL (1981) Efferent connections of the rat suprachiasmatic nucleus. Neurosci 6:2625–2641

    Google Scholar 

  • Stephan FK, Zucker I (1972) Circadian rhythms in drinking behavior and locomotor activity of rats are eliminated by hypothalamic lesions. Proc Natl Acad Sci USA 9:1583–1586

    Google Scholar 

  • Stetson MH, Watson-Whitmyre M (1976) Nucleus suprachiasmaticus: The biological clock in the hamster? Science 191:197–199

    Google Scholar 

  • Swanson LW, Cowan WM (1975) The efferent connections of the suprachiasmatic nucleus of the hypothalamus. J Comp Neurol 160:1–12

    Google Scholar 

  • Swanson LW, Kuypers HGJM (1980) The paraventricular nucleus of the hypothalamus: cytoarchitectonic subdivisions and organization of projections to the pituitary, dorsal vagal complex, and spinal cord as demonstrated by retrograde fluorescence double-labeling methods. J Comp Neurol 194:555–570

    Google Scholar 

  • Swanson LW, Sawchenko PE (1983) Hypothalamic integration: Organization of the paraventricular and supraoptic nuclei. Annu Rev Neurosci 6:269–324

    Google Scholar 

  • Swanson LW, Cowan WM, Jones EG (1974) An autoradiographie study of the efferent connections of the ventral lateral geniculate nucleus in the albino rat and the cat. J Comp Neurol 156:143–163

    Google Scholar 

  • Tamarkin L, Hutchison JS, Goldman BD (1976) Regulation of serum gonadotropins by photoperiod and testicular hormone in the Syrian hamster. Endocrinology 99:1528–1533

    Google Scholar 

  • Tigges J, Bos J, Tigges M (1977) An autoradiographic investigation of the subcortical visual system in chimpanzee. J Comp Neurol 172:367–380

    Google Scholar 

  • Turek FW (1983) Neurobiology of circadian rhythms in mammals. BioSci 33:439–444

    Google Scholar 

  • Turek FW, Campbell CS (1979) Photoperiodic regulation of neuroendocrine-gonadal activity. Biol Reprod 20:32–50

    Google Scholar 

  • Turek FW, Losee SH (1978) Melatonin-induced testicular growth in golden hamsters maintained on short days. Biol Reprod 18:299–305

    Google Scholar 

  • Turek FW, Elliott JA, Alvis JD, Menaker M (1975) Effect of prolonged exposure to nonstimulatory photoperiods on the activity of the neuroendocrine-testicular axis of the golden hamster. Biol Reprod 13:475–481

    Google Scholar 

  • Turek FW, Desjardins C, Menaker M (1976) Differential effects of melatonin on the testes of photoperiodic and nonphotoperiodic rodents. Biol Reprod 15:94–97

    Google Scholar 

  • Ueda S, Kawata M, Sano Y (1983) Identification of serotonin and vasopressin immunoreactivities in the suprachiasmatic nucleus of four mammalian species. Cell Tissue Res 234:237–248

    Google Scholar 

  • van den Pol AN (1980) The hypothalamic suprachiasmatic nucleus of rat: Intrinsic anatomy. J Comp Neurol 191: 661–702

    Google Scholar 

  • van den Pol AN, Powley T (1979) A fine-grained anatomical analysis of the role of the rat suprachiasmatic nucleus in circadian rhythms of feeding and drinking. Brain Res 60:307–326

    Google Scholar 

  • Zigmond RE, Baldwin C, Bowers CW (1981) Rapid recovery of function after partial denervation of the rat pineal gland suggests a novel mechanism for neural plasticity. Proc Natl Acad Sci USA 78:3959–3963

    Google Scholar 

Download references

Author information

Author notes

  1. Gary E. Pickard

    Present address: Institute of Neuroscience, University of Oregon, 97403, Eugene, OR, USA

Authors and Affiliations

  1. Department of Anatomy and Cell Biology, Columbia University, College of Physicians and Surgeons, 10032, New York, New York, USA

    Gary E. Pickard & Fred W. Turek

  2. Department of Neurobiology and Physiology, Northwestern University, 60201, Evanston, Illinois, USA

    Gary E. Pickard & Fred W. Turek

Authors
  1. Gary E. Pickard
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Fred W. Turek
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Pickard, G.E., Turek, F.W. Effects of partial destruction of the suprachiasmatic nuclei on two circadian parameters: wheel-running activity and short-day induced testicular regression. J. Comp. Physiol. 156, 803–815 (1985). https://doi.org/10.1007/BF00610832

Download citation

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00610832

Keywords

Search

Navigation